The Face as a Sensory Organ 2 - pdfs.semanticscholar.org implications of sensory–motor...

M.Z. Siemionow (ed.), The Know-How of Face Transplantation, 11 DOI: 10.1007/978-0-85729-253-7_2, © Springer-Verlag London Limited 2011

Abstract The human face is a highly specialized organ which receives sensory information from the environment and transmits it to the cortex. The advent of facial transplantation has recently shown that excel-lent reconstruction of disfiguring defects can be achieved; thus, the expectations are now focused on functional recovery of the transplant. So far, restora-tion of the facial sensation has not received the same attention as the recovery of motor function. We describe the current knowledge of the sensory pathways of the human face and their respective functions, the avail-able methods of sensory assessment, and the data on normal sensation. The topographical sensory anatomy of facial subunits is summarized, the trigemino-facial connections are illustrated, and the implications of these anatomical variations on facial allotransplanta-tion are emphasized.

2.1 Introduction

Since 2005, 11 reports on face transplantation have con-firmed that this procedure is technically and immuno-logically feasible. The goal of reconstructing severely disfiguring facial defects by coverage with similar tis-sues coming from human donors has been achieved. This opened the discussion on the best approach to achieve functional recovery of the transplanted face with restoration of fine facial movements and sensation. These two determinants of optimal functional recovery were restored differently for documented cases of face transplantation. In three patients, the facial nerve was repaired either directly (two patients)1 or with inter-positional nerve grafts (one patient),2-4 whereas the sen-sory nerves were satisfactorily repaired only in one case.1 These differences in the reconstructive approaches

The Face as a Sensory Organ

Maria Z. Siemionow, Bahar Bassiri Gharb, and Antonio Rampazzo

M.Z. Siemionow (*) Department of Plastic Surgery, Cleveland Clinic, Cleveland, OH, USA e-mail: [email protected]

2

Contents

2.1 Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11

2.2 Facial Skin Receptors and Their Function . . . . . 12

2.3 Physiology of Facial Sensation . . . . . . . . . . . . . . . 132.3.1 Light Touch . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 132.3.2 Temperature and Pain . . . . . . . . . . . . . . . . . . . . . . . 13

2.4 The Ascending Pathways of Facial Sensation . . . 13

2.5 The Peripheral Pathways of Facial Sensation . . . 142.5.1 Trigemino-Facial Communications . . . . . . . . . . . . . 14

2.6 Evaluation of Facial Cutaneous Sensibility, Temperature, and Pain Thresholds . . . . . . . . . . . 15

2.7 Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21

12 M.Z. Siemionow et al.

to motor and sensory nerve repairs were mainly dictated by the extent of facial trauma before transplantation.

One of the fundamental functions of the human face is the ability to receive multimodal sensory information from the environment and to convey it to the cerebral cortex for integration and processing. The presence of normal sensation is important not only for the discrimi-nation of touch, temperature, and pain, but also for ini-tiation of vigilant or defense reactions. The presence of labial sensation helps in avoiding drooling while eating or drinking.5 Stretching of the perioral skin contributes to the precise articulation in speech.6 Interestingly, cutaneous stimulation increases the intensity of esti-mates of the olfactory system.7 It has also been reported that facial skin cooling decreases the heart rate and increases blood pressure.8 Finally, normal sensory pathways allow to draw pleasure and satisfaction when exposed to external stimuli.9 It is clear that restoration of the above functions is expected and essential for the optimal outcomes following face transplantation.

To learn more about the importance of the face as a sensory organ, the aim of this chapter is to illustrate the complexity of the sensory pathways of the face and their specific functions, to review current methods of assess-ment of facial sensation, and to summarize the available data on normal sensation. Finally, the topographical sensory anatomy of facial subunits is summarized and the implications of sensory–motor communications on the mechanism of recovery of facial sensation after trauma and face allotransplantation are discussed.

2.2 Facial Skin Receptors and Their Function

Over 17,000 corpuscles have been reported in the human face, which contribute to several sensory func-tions.10 For the discrimination of touch, four different types of receptors have been described in the hairy skin of the face and include Ruffini corpuscles, Meissner corpuscles, Merkel cell disks, and hair recep-tors (Fig. 2.1).

Ruffini corpuscles are especially sensitive to skin stretch, consist of axon terminals and surrounding Schwann cells that envelop tightly bundles of collagen fibrils and are associated with vellus hairs. They are innervated by the superficial portion of the dermal neural network.

Meissner corpuscles are more sensitive to stroking and fluttering of the skin and are localized in the dermal papillae. They are globular fluid-filled structures enclos-ing a stack of flattened epithelial cells. The terminal axons are entwined between the various layers of the corpuscles.

The Merkel disk receptors are formed by a small epithelial cell surrounding the nerve endings. Merkel receptors detect pressure applied on the skin and dis-criminate texture of objects. Two different types of Merkel cells have been described in facial skin.11 The first type is localized in the dermis, on the external root sheath collar; it is not associated with nerve terminals and it is undifferentiated. The Merkel cells localized in the basal layer of the epidermis are associated with nerve terminals and have different granules within a single cell. An endocrine function has been attributed to them via regulation of the autonomic nerves.12

Interestingly, the Pacini corpuscles, which are well described in the fingertips and the palm of the hand where they are responsible for detection of vibrations, are absent in the skin of the human face.12-14

Hair follicle fibers work in a similar way to Meissner corpuscles, displaying a lower threshold for light strok-ing. They form a palisade of lanceolate terminals, which abut the external root sheath of the vellus hair in

Fig. 2.1 The receptors of the human facial skin. MSC meissner corpuscle, FNE free nerve endings, MRD merkel disk, RC ruffini corpuscle, HFF hair follicle fiber (Reprinted with permission, Cleveland Clinic Center for Medical Art & Photography © 2010. All Rights Reserved)

132 The Face as a Sensory Organ

the region of the follicular neck. They derive from the deeper portion of dermal nerves.15

Beyond nerve fibers connected to mechanoreceptors and hair follicles, there are also free nerve endings with sensory function (temperature and pain). The intraepi-dermal nerve fibers terminate in different cellular lay-ers, although the majority reach the stratum granulosum. The distribution of these endings is focal.16,17 Kawakami et al.16 reported that face presents with the highest dis-tribution density of the free nerve endings. It was reported that beyond the sensory role, they may have also a trophic or immunoregulatory function.17,18

2.3 Physiology of Facial Sensation

2.3.1 Light Touch

The response of the face to the light touch is mediated by facial mechanoreceptors. These are associated with Ab fibers (myelinated, 10–15 mm in diameter), divided into slowly and quickly adapting units. Slowly adapt-ing axons initiate neural signals as soon as the skin is stimulated and continue to generate them as long as the cutaneous stimulus is sustained. Ruffini complexes and Merkel cell disks are the terminal corpuscles that are associated with these nerve fibers.19

Quickly adapting nerve fibers are activated only when new stimuli are applied. Hair follicle fibers and Meissner corpuscles are involved in transduction of these signals.19,20 Innervation density for both quickly and slowly adapting fibers has been reported to increase from the upper face to the mid-face, followed by the lower face and the lip.19

Receptive field sizes of the facial skin afferents have been described to be similar in dimension to the recep-tive fields of the afferents innervating the vermilion (7–8 mm2)12 and the highest concentration of facial mechanoreceptors has been found at the corners of the mouth.21

2.3.2 Temperature and Pain

The perception of temperature changes and painful stimuli delivered to facial skin is not mediated by cor-puscled receptors, but by small myelinated (Ad) and

unmyelinated fibers (C fibers). The cold receptors increase the firing rate with decreases in temperature, while warmth receptors increase the firing rate with increased temperature. In a study by Davies et al.,22 raising of the temperature between 35°C and 40°C evoked a sensation of warming. In contrast, the cold receptors increased activity at lower temperatures ranging between 35°C and 15°C.

Nociceptors of the face are responsible for central transmission of painful stimuli and are activated by high threshold skin indentations (23 or 51 g),23 as well as temperatures below 0°C24 or above 47°C.25

2.4 The Ascending Pathways of Facial Sensation

The ascending pathways transmit the somatosensory information collected by the facial receptors, and con-veyed by the peripheral axons of the trigeminal sen-sory neurons (along the peripheral pathways), to higher cortical centers for processing and integration.26 These primary sensory neurons reside in the trigeminal gan-glion (Gasser’s ganglion or Ganglion Semilunaris) in the middle cranial fossa, from which afferent fibers pass into the mid-pons27 (Fig. 2.2). The second order sensory neurons reside in trigeminal sensory nucleus. The sensory nucleus is divided into three subnuclei: the principal sensory nucleus is located in the pons and mediates facial light touch and pressure sensation; the mesencephalic nucleus, which receives proprio-ceptive information from the masticator muscles and the nucleus of the spinal tract, extends into the upper cervical cord (C2–C4) and is responsible for transmis-sion of facial pain and temperature and secondarily facial touch.28,29 After entering the pons, the pain and temperature fibers run caudally, forming the descend-ing trigeminal tract and synapse with the second order neurons of the spinal nucleus. The axons of these neu-rons cross the midline and extend to the controlateral ventral posteromedial (VPM) nucleus of the thalamus, forming the ventral trigeminothalamic tract (or lem-niscus).30 Sensory fibers mediating light touch synapse in the principal sensory nucleus.31 The secondary neu-ron axons ascend to the VPM nucleus of thalamus either contralaterally in the ventral trigeminothalamic tract (most) or ipsilaterally (dorsal trigeminothalamic tract)29,30,32 (Fig. 2.2).


From the ventroposteromedial thalamic nucleus, a third relay of fibers, the thalamocortical tract in the internal capsule, passes to the extensive face area of the main sensory neocortex (S-1 and S-2) of the post cen-tral gyrus (Brodman areas 3, 1, 2) and the upper bank of the sylvian fissure32 (Fig. 2.2). Penfield reported that the representation of the facial structures was organized along the central sulcus, with the forehead in the super-omedial region adjacent to the hand area, and the chin in the33 inferolateral region.33 The order of representa-tion of the different facial subunits has been subject of debate. Tamura et al.34 found, by using somatosensory-evoked magnetic fields, that topography of the areas representing intraoral structures along the central sul-cus was the index finger, upper or lower lip, anterior or posterior tongue, and superior or inferior buccal mucosa, with a wide distribution, covering 30% of the S1 cortex. The skin-covered areas of the face were recently “relocated” between the thumb and the lip,

which was in contrast to the original Penfield study.35 Current studies in monkeys showed evidence for an upside-down representation;36 however, studies by other investigators could not confirm either orientation.37

2.5 The Peripheral Pathways of Facial Sensation

The peripheral pathways, formed by the peripheral branches of the trigeminal sensory neurons, are respon-sible for conveying the sensory data from the facial skin to the Central Nervous System. The peripheral fibers of the primary sensory neurons exit the trigemi-nal ganglion organized into three trunks: the ophthal-mic (V1), the maxillary (V2), and the mandibular (V3) nerves. The former two are purely sensory, whereas the latter is a mixed sensory and motor nerve. The trigeminal nerve collects sensibility of the full face except a small area around the mandibular angle and the auricular lobe, which is innervated by the great auricular nerve (C2–C3) (Fig. 2.3). The branches of these nerves supply sensation to the facial subunits of the upper face, mid-face, and lower face as summa-rized in Tables 2.1–2.3.

2.5.1 Trigemino-Facial Communications

When assessing the sensory recovery after facial trauma or transplantation, it is important to take into consideration the existence of direct connections between trigeminal nerve and facial nerve, which may play an important role in the mechanisms of facial sen-sory recovery.

The cutaneous branches of all three divisions of the trigeminal nerve and of the great auricular nerve show plexiform connections with the terminal rami of the facial nerve (Fig. 2.4). These connections can occur either in the proximal (auriculotemporal, great auricu-lar) or distal (supraorbital, infraorbital, buccinators, mental) region of the facial nerve distribution. The auriculotemporal connections, to the upper division of the facial nerve, are the most consistent and sizable and represent the most constant pattern of the trigem-ino-facial communications.38,39

Fig. 2.2 Ascending pathways of facial sensation are shown from the peripheral branches of the trigeminal nerve which col-lect the sensory information and convey it to the Central Nervous system. OPN ophtalmic nerve, MXN maxillary nerve, MAN mandibular nerve, TG trigeminal ganglion, MST+MSN mesen-cephalic tract and nucleus, MN main sensory nucleus, DST+SN descending spinal tract and nucleus, VTTT ventral trigeminotha-lamic tract, DTTT dorsal trigeminothalamic tract, Th thalamus, VPM ventral posteromedial nucleus of thalamus (Reprinted with permission, Cleveland Clinic Center for Medical Art & Photography © 2010. All Rights Reserved)


There is no common agreement on the function of the nerve fibers in the communicating rami. O’Connell and Huber reported that the relationship was of mere contiguity and after a joint journey, the sensory branches separated from the motor branches, each ele-ment finding the tissue it was destined to supply.40,41 Others suggested that the trigeminal nerve fibers, in the communicating rami, conveyed proprioceptive information regarding the mimetic muscles, and the pseudomotor fibers to the integument or secretomotor fibers to the superficial part of the parotid and buccal mucosa glands.42 Baumel implied43 that sympathetic

and parasympathetic fibers, not belonging to the trigeminal nerve, may also be the constituents of the communicating rami.

Finally, some investigators hypothesized pres-ence of a sensory component in the facial nerve which explained the preservation of deep facial sen-sation after trigeminal neurectomy.44,45 The connec-tions between the facial nerve and the branches of the trigeminal and cervical nerves could also pro-vide an additional motor supply to the superficial facial musculature.41

2.6 Evaluation of Facial Cutaneous Sensibility, Temperature, and Pain Thresholds

Current methods of sensibility testing evaluate the fiber–receptor complexes that mediate the perception of touch, temperature, and pain. Pressure thresholds (Semmes–Weinstein monofilament test) and static two-point discrimination (Disk-Criminator, Pressure-Specified Sensory Device) assess the function of slowly adapting fibers associated with Ruffini recep-tors and Merkel cell disks.19,20 Tactile discrimination reflects the number of innervated sensory receptors. Moving two-point discrimination and vibration stimuli (Tuning fork) assess the function of quickly adapting nerve fibers, hair follicle fibers, and Meissner corpus-cles.19,20 Perception of two-point discrimination, vibra-tion, and pressure threshold values improves from the lateral and posterior areas of the face to the midline, with the vermilion being the most sensitive area and the forehead being the least sensitive.46,47 Table 2.4, summarizes the values of normal ranges for tactile dis-crimination of the human face.

Two-point discrimination and vibratory values in females are reported to be lower when compared to males, although these differences are not statistically significant. There are also no significant differences between left and right side of the human face.46,48,49 Interestingly, all of the tests evidence higher values for smokers and subjects older than 45 years of age.19,46

The facial skin is relatively uniform in its sensitivity to warming. In response to thermal stimuli, the infraor-bital region and nose are the most sensitive to warm-ing, whereas other areas of the face do not differ

Fig. 2.3 Sensory innervation of the human face. BN buccal nerve, ENb-AEN external nasal branch-anterior ethmoidal nerve, GA great auricular nerve, Hb-SON horizontal branch supraorbital nerve, ION infraorbital nerve, ITN infratroclear nerve, MN mental nerve, mylohyoid branch-mental nerve, Pb-LN palpebral branch-lacrimal nerve, SON supraorbital nerve, STN supratroclear nerve, ZFN zygomaticofacial nerve, ZTN zygomaticotemporal nerve (Reprinted with permission, Cleveland Clinic Center for Medical Art & Photography © 2010. All Rights Reserved)


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poro

man

dibu

lar

join

t

Ant

erio

r au

ricu

lar

nerv

e an

d th

e ex

tern

al

acou

stic

mea

tus

nerv

e

Lat

eral

to n

eck

of

man

dibl

e, p

erfo

rate

su

perfi

cial

tem

pora

l fa

scia

Aur

icul

ar a

nter

ior

aspe

ct,

exte

rnal

aco

ustic

mea

tus

Gre

at a

uric

ular

ne

rve

(C2–

C3)

Supe

rfici

al b

ranc

h of

the

cerv

ical

ple

xus

(C2–

C3)

Erb

’s p

oint

Ant

erio

r an

d po

ster

ior

bran

ches

Plat

ism

a m

uscl

ePa

rotid

gla

nd a

nd th

e lo

wer

pr

eaur

icul

ar r

egio

n80

Tab

le 2

.2 S

enso

ry in

nerv

atio

n of

the

mid

-fac

e in

clud

ing:

low

er e

yelid

s, n

ose,

upp

er li

ps, c

heek

, and

pre

auri

cula

r ar

ea


significantly from one another.50 There are not signifi-cant differences in sensitivity to cooling between oral mucosa and facial skin. Moreover, all extraoral sites are equally sensitive to cooling.51

In comparison to the above discussed neurosensory tests, the pain detection threshold represents the high-est variability in data. Upper and lower labial areas are

the most sensitive to pain stimuli, and the infraorbital areas are the least sensitive. In comparison, chin responses are in between these two areas.52 The rea-sons for these spatial variations are undoubtedly numerous and most probably correlate with innerva-tions density, epidermal thickness, and composition as well as with the receptors’ depth.

Nerve Origin Exit foramen Branches Structures crossed

Areas innervated

Lower eyelids, cheek and upper lips

Mental (V3) Terminal branch of the inferior alveolar nerve (from the mandibular nerve) (V3)

Mental foramen81,82

Angular, medial inferior labial, lateral inferior labial, and mental branch

Depressor Anguli Oris muscle

Lower lip, vermilion, vestibular gengiva, and the skin of the chin

Branch of the mylohyoid nerve (V3)

Terminal branch of the mandibular nerve (V3)74,83

None None Mylohyoid muscle

Submental skin

Table 2.3 Sensory innervation of the lower face including: lower lips and chin

Fig. 2.4 Trigemino-facial communications. The trigeminal nerve and its branches are presented in yellow, the facial nerve in orange, and their communicating branches in blue. BB buccal branch of the facial nerve, BN buccal nerve, CB cervical branch of the facial nerve, ENb-AEN, external nasal branch-anterior ethmoidal nerve, FTB frontotemporal branch of the facial nerve, GA great auricular nerve, Hb-SON horizontal branch supraor-bital nerve, ION infraorbital nerve, ITN infratroclear nerve,

MMB marginal mandibular branch of the facial nerve, MN men-tal nerve, mylohyoid branch-mental nerve, Pb-LN palpebral branch-lacrimal nerve, SON supraorbital nerve, STN supratro-clear nerve, ZB zygomatic branch of the facial nerve, ZFN zygo-maticofacial nerve, ZTN zygomaticotemporal nerve (Reprinted with permission, Cleveland Clinic Center for Medical Art & Photography © 2010. All Rights Reserved)


Lat

eral

fo

rehe

adM

edia

l fo

rehe

adZ

ygom

aC

heek

Nas

olab

ial

skin

Para

nasa

lSu

peri

or

labi

al s

kin

Upp

er

verm

ilion

Upp

er li

p m

ucos

aIn

feri

or

labi

al s

kin

Low

er

verm

ilion

Low

er li

p m

ucos

aC

hin

Ear

Nec

k

Two-

poin

t di

scri

min

atio

n (s

tatic

)

13.4

, 15

.012

.7,

13.0

10.5

8,

10.9

29.

0,

13.1

7.4,

9.

79.

96,

10.3

83.

25,

7.66

2.4,

7.

02.

4,

5.2

5.8,

7.

043.

0,

6.1

2.8,

4.

65.

4,

10.0

9.29

, 13

.213

.7,

35.2

Two-

poin

t di

scri

min

atio

n (d

ynam

ic)

11.0

, 11

.89.

0,

11.1

9.33

, 9.

917.

9,

10.0

6.6

9.63

, 10

.17

3.42

, 3.

84.

26.

14.

53.

0, 4

.17.

0,

5.1

12.9

11.5

Sem

mes

-Wei

nste

in

(fila

men

t)1.

951.

931.

72,

1.84

1.75

1.75

, 1.

812.

382.

81.

75,

1.77

2.26

2.91

1.95

1.79

, 1.

992.

13

Vib

rato

ry

thre

shol

d (v

olta

ge,

mV

)

22.0

, 22

.521

.0,

22.8

17.0

, 17

.215

9.8

8.3

9.4

8.1

6.0,

9.3

11.0

, 10

.611

.311

.9

Pres

sure

-spe

cifie

d se

nsor

y de

vice

1-

poin

t sta

tic

(g/m

m)

0.88

, 1.

160.

88,

0.95

0.71

, 0.

780.

76,

0.80

0.77

, 0.

820.

73,

0.77

0.69

, 0.

780.

64,

0.82

Pres

sure

-spe

cifie

d se

nsor

y de

vice

2-

poin

t sta

tic

(g/m

m)

31.1

1,

39.4

222

.94,

33

.38

20.5

8,

23.1

13.3

9,

13.5

311

.08,

13

.07

3.8,

3.

983.

27,

3.57

16.8

8,

17.1

8

Pres

sure

-spe

cifie

d se

nsor

y de

vice

1-

poin

t mov

ing

(g

/mm

)

0.58

, 0.

710.

56,

0.88

0.54

, 0.

580.

54,

0.55

0.51

, 0.

570.

49,

0.52

0.47

, 0.

540.

52,

0.62

Pres

sure

-spe

cifie

d se

nsor

y de

vice

2-

poin

t mov

ing

(g

/mm

)

10.1

6,

11.7

85.

27,

8.23

5.2,

5.

473.

45,

3.72

2.66

, 4.

681.

10,

1.15

1.13

, 1.

312.

52,

4.28

Tab

le 2

.4 P

hysi

olog

ic ta

ctile

dis

crim

inat

ion

data

for

dif

fere

nt a

reas

of

the

hum

an f

acia

l ski

n19,2

0,46

,48,

49,5

2,84


2.7 Conclusions

With 11 reported cases of facial allotransplantation, the technical challenges seem to be well addressed. The new challenges include achieving long-term survival under minimal immunosuppression and restoration of optimal sensory and motor functions after face trans-plantation. The motor function recovery after face trans-plantation is well documented and discussed, but the mechanisms of sensory recovery have not been ade-quately addressed. The presence of stable and diffuse connections between the facial and trigeminal nerves proves that the motor and sensory pathways of the human face are intrinsically interrelated; thus, every effort should be made to restore the continuity of both systems. The new era of facial reconstruction includes free tissue transfer and facial transplantation, so updating our knowledge on the sensory pathways of the face, includ-ing specific facial receptor systems, the ascending tracts, and the cortical responses to somatosensory stimulations, should add into our understanding of function and mechanisms of sensory restoration after application of modern reconstructive procedures. The facial skin presents the highest concentration of the sensory receptors in the entire body,10 as confirmed by their fundamental role in collecting and transmitting external stimuli to the cerebral cortex for processing and integration. In contrast to the significant number of studies on composition and distribution of the sen-sory receptors within the hand, there are only few reported anatomical studies, performed principally on nonhuman primates, assessing the spectrum of recep-tors present in the facial skin. Only Munger and Halata15 described the complex array of sensory recep-tors in the human face. There are, however, numerous micro-neurographic studies which confirmed the pres-ence of four out of five types of tactile afferents which are known to innervate skin of the human hand as well, and excluded the presence of Pacini corpus-cles.12,14,21 For clinical evaluation of the sensation col-lected by facial receptors, different instruments and assessment devices have been described, but none of the tests have been accepted as the gold standard. Pressure-Specified Sensory Device (PSSD) is proba-bly the most appropriate instrument for recording of human cutaneous pressure thresholds by measuring both the force and the distance at which one point can be distinguished from two points either static or mov-ing.47 Tests for thermal sensation are difficult to

standardize since their accuracy and reliability have not been well determined.53 Perception of the painful stimuli is usually not used in the clinical practice of sensory testing but has often been inferred from the necessity for local anesthesia when performing skin biopsies2 or by pinprick tests. Based on previous reports, the presented summary of the range of normal values for discriminative thresholds may be useful for assessment of sensory recovery of facial sensation after free tissue transfers and in face transplant patients, since these tests are not routinely used in the current clinical practice. The reported higher tactile thresholds in patients older than 45 and in smokers should be taken into consideration during evaluation of sensibil-ity of reconstructed or transplanted face especially if the donor age is different from the age of the recipient. During evaluation of sensory function return of a spe-cific nerve branch, the areas to be tested should be scaled purely to the region of the repaired nerve distri-bution. For example, the middle third of the hemi-fore-head should be tested for assessment of the supraorbital nerve, the central cheek and upper lip for the assess-ment of the infraorbital nerve, and the lower lip for the mental nerve. When testing thermal stimuli, the infraorbital region and nose should be considered as they were found to be the most sensitive to warm stim-uli.51 Upper and lower labial regions have been reported to be most sensitive to pain and if required can be used for assessment of painful stimuli while the infraorbital regions are the least sensitive52 and should be avoided during sensory testing.

The distribution of the sensory nerves in the human face is usually described as a branching pattern from the main trunk to the distal rami. This approach is not helpful for sensory assessment from a reconstructive point of view, where focusing on the “complex” of peripheral nerves directly involved in the innervation of the reconstructed subunit would be more valuable. The summary offered in the Table 2.1 may be useful as a guide when deciding which is the most suitable area for sensory testing and which nerves should be consid-ered for repair in composite unit transfers. Furthermore, the following anatomical features should be consid-ered when repairing sensory nerves after trauma or during face transplantation. It is important to consider the fact that the supraorbital nerve exits the cranium through a bony foramen or notch, and multiple foram-ina have been reported. A high positioned supraorbital foramen with a long bony canal can be present in up to


24% of cases.54 Moreover, the medial branch of the supraorbital nerve after exiting the foramen gives off multiple small rami and becomes superficial piercing the frontalis muscle. The infraorbital and mental nerves pass through long bony canals. They are already divided into their terminal branches at the level of foraminal exit, and they have a short distance to reach the skin. The presence of multiple foramina or rami, the long bony canals, and the short course of the main branches within soft tissues after exiting the cranium explains the reported difficulty in achieving direct repair of the sensory nerves in facial trauma and facial transplantation.2 Osteotomy of the supraorbital canal, as proposed by Siemionow et al.,55 or intraorbital divi-sion of the nerve and delivery of the proximal stump through the canal,54 could be performed to lengthen the stump of the nerve available for repair. The infraorbital canal osteotomy and mandibular sagittal osteotomy are also useful to increase the length of these nerves during facial graft procurement.55

Beside the primitive reflex functions which aim to protect the individual from the noxious stimuli, the unconscious information conveyed by the trigeminal system assists in the fine tuning of the highly special-ized facial functions. Livermore et al.7 proved that the stimulation of the facial skin increases the perceived intensity of chemical stimuli applied simultaneously to the olfactory system. The stimulation of the trigem-inal nerve has been shown to evoke systemic visceral reactions, when e.g., cooling of the face was associ-ated with hypertension and bradycardia.8 Finally, due to the absence of muscle spindles and tendon organs in the perioral muscle system,56,57 the cutaneous receptors play an important role in the speech senso-rimotor processes and adjustment of the articular motion.6 The cutaneous and mucosal afferents dis-charge vigorously during labial contact and when stimulated by the air pressure, generated by speech sounds. Deformation or strain of the facial skin and mucosa associated with various phases of voluntary lip and jaw excursions provides proprioceptive infor-mation on facial movements.58

The second important aspect to consider is the response of the somatosensory cortex to the recon-struction of the sensory nerves. It has been proved that cortical reorganization following limb deafferen-tation involves reduction of the cortical representa-tion in the motor and sensory cortices, with expansion of adjacent and controlateral areas.59,60 Studies on the

reorganization of the somatosensory cortex in patients undergoing hand transplantation showed the revers-ibility of this phenomenon. The patients showed acti-vation of the primary somatosensory cortex, which started as early as 10 days and was observed61 up to 2 years following transplantation.62 Interestingly, Farne et el.63 confirmed that the somatosensory per-ception of the transplanted hand was hampered when the ipsilateral face was simultaneously stimulated. This phenomenon disappeared 11 months after trans-plantation. During the remapping phase, when the transplanted hand reclaimed its original somatotopy, the face and the hand seemed to “compete” for the cortical representation and gave rise to a temporary overlapping area that received multiple conflicting inputs from two physically distant but cortically adja-cent parts of the body. Equivalent modifications of the somatosensory cortex have not been studied in the face transplant patients. It would be interesting to evaluate if opposite changes can be detected. These findings are very important in the light of current attempt of simultaneous face and hand transplanta-tion where potential competition for critical reeduca-tion may take place jeopardizing functional outcome of one of the transplanted grafts.

In conclusion, we have illustrated the complexity of the sensory pathways of the human face and presented the role of facial sensation during interaction with the external environment. We believe that considering the present advancements in the field of facial transplanta-tion, restoration of facial anatomy and function is cru-cial for the final outcome.

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